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A more recent version of this article appeared on August 11, 2000
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Papers In Press, published online ahead of print June 5, 2000
J. Biol. Chem, 10.1074/jbc.M906729199
Submitted on August 22, 1999
Revised on April 13, 2000
Accepted on June 5, 2000

Membrane-embedded synaptotagmin penetrates cis or trans target membranes and clusters via a novel mechanism

Jihong Bai, Cynthia A. Earles, Jessica L. Lewis, and Edwin R. Chapman

Department of Physiology, University of Wisconsin-Madison, Madison, WI 53706

Corresponding Author: chapman{at}physiology.wisc.edu

The synaptic vesicle protein synaptotagmin I has been proposed to serve as a Ca2+-sensor for rapid exocytosis. Synaptotagmin spans the vesicle membrane once and possesses a cytoplasmic domain largely comprised of two C2-domains designated C2A and C2B. We have determined how deep the Ca2+-binding loops of Ca2+-C2A penetrate into the lipid bilayer and report mutations in synaptotagmin that can uncouple membrane-penetration from Ca2+-triggered interactions with the SNARE-complex. To determine whether C2A penetrates into the vesicle ("cis") or plasma ("trans") membrane, we reconstituted a fragment of synaptotagmin that includes the membrane-spanning and C2A-domain (C2A-TMR) into proteoliposomes. Kinetics experiments revealed that cis interactions are rapid (< 500 µsec). Binding in the trans mode was distinguished by the slow diffusion of trans target vesicles. Both modes of binding were observed, indicating that the linker between the membrane anchor and C2A-domain functions as a flexible tether. C2A-TMR assembled into oligomers via a novel N-terminal oligomerization domain suggesting that synaptotagmin may form clusters on the surface of synaptic vesicles. This novel mode of clustering may allow for rapid Ca2+-triggered oligomerization of the protein via the membrane distal C2B-domain.


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